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Diversity, stability, productivity, and policing

This week I will discuss two papers, both of which consider possible benefits of biological diversity. In interpreting the data in the experimental paper, on bees, we need to remember that a given set of data can often be consistent with two or more different hypotheses. This point is reinforced in the review article, which discusses the relationship between diversity and stability of ecosystems.

The experimental paper is "Genetic diversity in honey bee colonies enhances productivity and fitness" by Heather Mattila and Thomas Seeley, of Cornell University (Science 317:362). The review article is "Stability and diversity of ecosystems" by Anthony Ives and Stephen Carpenter, of the University of Wisconsin (Science 317:58).

Any hypothesis worthy of the name makes predictions. Testing these predictions may take a long time or lots of money. Edmond Halley's 1716 prediction that a transit of Venus could be used to measure the distance to the sun could not be tested until the next transits of Venus in 1761 and 1769, and required global scientific expeditions. (Mark your calendars for 6 June 2012!) The Rothamsted Experiment Station has been testing the hypothesis that wheat can be grown with only inorganic inputs and without rotating to other crops, since 1843. This may not be long enough to uncover all possible problems with inorganic fertilizers and continuous monoculture, but it's quite a contrast with an acquaintance who wrote that "I've been farming sustainably for three years."

If even one of a hypothesis's predictions turns out to be unambiguously wrong, the hypothesis must be discarded or revised. On the other hand, multiple correct predictions do not prove that a hypothesis is true -- there might be other hypotheses that make the same predictions. Either way, it's useful to consider several hypotheses, if you can.

Tom Kinraide and I discussed these points in an article in American Biology Teacher in 2003. His boss wouldn't let him include his USDA affiliation, because someone at the lab complained that testing hypotheses would undermine his religion. I don't know; maybe it would. But back to this week's papers...

Mattila and Seeley impregnated honey bee queens with the same total amount of sperm from either one or 15 male bees. The latter led to more genetic diversity among worker bees, as in most wild colonies. More diverse colonies usually foraged more actively and stored 39% more food. They also produced more female worker bees and more male drones.

What hypotheses can explain these results? Bees apparently vary genetically in the amount of stimulus they require to start foraging or other tasks. The authors suggested that more diverse colonies might "respond to a broad[er] range of task-specific stimuli", but noted that the treatments differed even when food reserves were so low that "stimuli reflecting these needs could not have been greater."

An alternative hypothesis is that genetic diversity would affect within-colony cooperation. The authors suggested that any such effect should be in the wrong direction, because greater genetic diversity "erodes high levels of relatedness among female offspring, thereby hindering the evolution of altruistic behavior toward kin", consistent with Hamilton's Rule.

But altruism towards which kin: their sisters or their mother, the queen? In an earlier analysis by Ratnieks (American Naturalist 132:217) noted that unfertilized worker bees can sometimes lay male eggs. He wrote that:

As the number of males that mate with a queen increases, the relatedness (G) between a worker and the male offspring of the queen remains constant (G = 0.25), whereas the mean relatedness between workers and the male offspring of other workers declines from 0.375 to 0.125... Therefore, it is hypothesized that an allele, referred to as a "police allele," that causes workers to favor the production of queen-produced males over worker-produced males (i.e., to police other workers) should spread in eusocial hymenopteran populations in which queens mate with many males. Increased reproductive harmony, in which worker reproduction is reduced, is, therefore (and counterintuitively), a possible outcome of lowered relatedness between workers.

If egg-laying workers forage less, then reduced altruism towards fellow workers (leading to policing) may be a benefit of increased diversity, not a cost.

Additional details on the behavior of the offspring of singly- versus multiply-mated queens could help distinguish between these hypotheses. At this point, it would be premature -- the authors have not done so -- to generalize from this study to any broader relationship between diversity and productivity.

The review article focuses on the relationship between species diversity and the stability of ecosystems, but most of their insights would also apply to other ecosystem-level properties, including productivity. Ives and Carpenter point out that there are many ways to measure stability, and different measures can lead to opposite conclusions. Consistent with my comments above about hypotheses, they say:

it is not sufficient for theory to predict correctly whether the diversity-stability relationship is positive or negative; models could give the right prediction for the wrong reasons. Instead, theoretical models must be judged by their ability to capture the entire dynamics of the empirical system.
They also call for more explicit consideration of mechanisms by which diversity might affect stability, because
if the mechanisms underlying diversity-stability relationships are not identified, it is unclear whether an observed diversity-stability relationship can be generalized to any other system.

For example, research by colleagues here at the University of Minnesota found that, although the number of plant species had no statistically significant effect on soil nitrate levels, nitrate was significantly lower when there were more distinct functional categories of plants (Science 277:1300). Lower nitrate levels in the soil mean less risk of nitrate pollution in rivers and groundwater. Can we generalize from these results to other ecosystems, possibly including agriculture?

Ives and Carpenter might say that it would depend on the whether the mechanism linking functional diversity to lower nitrate applies to other ecosystems. For example, if less diversity meant that roots were inactive (not taking up nitrate) more months of the year, then you might expect a similar pattern in other ecosystems with a similar pattern.

But what I noticed, in visiting the research plots, was that at least some of the single-species plots had lots of bare soil, not shaded by any plants. This contrasts with other ecosystems dominated by a single species (redwood forests, say, or corn fields), which often have fairly complete plant cover. Of course, some differences between ecosystems might be irrelevant to the diversity-nitrate relationship. But I agree with Ives and Carpenter: more rigorous testing of hypotheses that explicitly include mechanisms will lead to faster scientific progress.

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